Summary
Retrograde neuronal tracing with the fluorescent dye True Blue and immunocytochemistry were utilized to examine postganglionic sympathetic neurons in para- and prevertebral ganglia projecting to the rat ovary. Perikarya in both ganglia were labeled with True Blue after application of the tracer to either the superior ovarian or ovarian plexus nerve. After application of True Blue to the superior ovarian nerve, 17% of the labeled cells in paravertebral ganglia were immunoreactive for vasoactive intestinal polypeptide. In contrast, after application of True Blue to the ovarian plexus nerve, approximately 1 % of the labeled cells in paravertebral ganglia were immunoreactive for the same polypeptide. Some vasoactive intestinal polypeptide-immunoreactive perikarya in paravertebral ganglia were not labeled with True Blue. In some cases, substance P- and vasoactive intestinal polypeptide-immunoreactive fibers were closely apposed to True Blue-labeled perikarya in para-and prevertebral ganglia. Paravertebral vasoactive intestinal polypeptide-immunoreactive perikarya projecting to the ovary presumably participate directly in the control of various ovarian functions. Substance P- and vasoactive intestinal polypeptide-immunoreactive fibers closely apposed to perikarya projecting to the ovary may participate indirectly in the control of various ovarian functions by affecting the activity of ovarian postganglionic neurons.
Similar content being viewed by others
References
Ahmed CE, Dees WL, Ojeda SR (1986) The immature rat ovary is innervated by vasoactive intestinal peptide (VlP)-containing fibers and responds to VIP with steroid secretion. Endocrinology 118:1682–1689
Baker SC, Cuello AC, Matthews M (1980) Substance P-containing synapses in a sympathetic ganglion and their possible origin as collaterals from sensory nerve fibres. J Physiol 308:76P-77P
Barr M Jr, Hensh RP, Brent RL (1970) Prenatal growth in the albino rat: Effects of number, intrauterine position and resorptions. Am J Anat 128:413–428
Beers WH, Strickland S, Reich E (1975) Follicular plasminogen and plasminogen activator and the effect of plasmin on ovarian follicle wall. Cell 6:379–386
Buchanan GD (1974) Asymmetrical distribution of implantation sites in the rat uterus. Biol Reprod 11:611–618
Burden HW, Lawrence IE Jr, Smith CP Jr, Hoffman J, Leonard M, Fletcher DJ, Hodson CA (1986) The effects of vagotomy on compensatory ovarian hypertrophy and follicular activation after unilateral ovariectomy. Anat Rec 214:61–66
Carlsson B, Törnell J, Hillensjö T (1987) Vasoactive intestinal peptide stimulates meiosis of follicle-enclosed rat oocytes in vitro. Acta Physiol Scand 129:437–439
Clark KE, Mills EG, Stys SJ, Seed AE (1981) Effects of vasoactive polypeptides on the uterine vasculature. Am J Obstet Gynecol 139:182–188
Coons AH, Leduc FH, Connolly JM (1955) Studies on antibody production. I. A method for the histochemical demonstration of specific antibody and its application to the study of the hyperimmune rabbit. J Exp Med 102:49–60
Dalsgaard CJ, Hökfelt T, Elfvin L-G, Terenius L, Emson P (1981) Tracing of substance P and enkephalin immunoreactive neurons projecting to the guinea pig inferior mesenteric ganglion: Immunohistochemistry combined with fluorescent retrograde labelling. Neuroscience [Abstr] 7:101
Dalsgaard CJ, Hökfelt T, Elfvin L-G, Skirboll L, Emson P (1982) Substance P-containing primary sensory neurons projecting to the inferior mesenteric ganglion: Evidence from combined retrograde tracing and immunohistochemistry. Neuroscience 7:647–654
Dalsgaard CJ, Hökfelt T, Schultzberg M, Lundberg JM, Terenius L, Dockray GJ, Goldstein M (1983) Origin of peptide-containing fibers in the inferior mesenteric ganglion of the guinea pig: Immunohistochemical studies with antisera to substance P, enkephalin, vasoactive intestinal polypeptide, cholecystokinin and bombesin. Neuroscience 9:191–211
Davoren BJ, Hsueh AJW (1984) Vasoactive intestinal peptide (VIP) stimulates steroid biosynthesis by cultured rat granulosa cells. Excerpta Medica 7th Int Congr Endocrinol 652:490
Dees WL, Kozlowski GP, Dey R, Ojeda SR (1985) Evidence for the existence of substance P in the pre-pubertal rat ovary. II. Immunocytochemical localization. Biol Reprod 33:471–476
Dees WL, Ahmed CE, Ojeda SR (1986) Substance P-and vasoactive intestinal peptide-containing fibers reach the ovary by independent routes. Endocrinology 119:638–641
Del Fiacco M, Levanti MC, Contini M, Montisci R, Savona G, Brotzu G (1985) Localization of substance Pand enkephalinlike immunoreactivity in the human paravertebral sympathetic ganglia. Bas Appl Histochem 29:309–320
Elfvin L-G, Dalsgaard CJ (1977) Retrograde axonal transport of horseradish peroxidase in afferent fibers of the inferior mesenteric ganglion of the guinea pig. Identification of the cells of origin in dorsal root ganglia. Brain Res 126:149–153
Gram BR, Ottesen B (1982) Increased myometrial blood flow evoked by substance P in non-pregnant rabbit. Pflügers Arch 395:347–350
Hökfelt T, Elfvin L-G, Elde R, Schultzberg M, Goldstein M, Luft R (1977a) Occurrence of somatostatin-like immunoreactivity in some peripheral sympathetic noradrenergic neurons. Proc Natl Acad Sci USA 74:3587–3591
Hökfelt T, Elvin L-G, Schultzberg M, Fuxe K, Said SI, Mutt V, Goldstein M (1977b) Immunohistochemical evidence of vasoactive intestinal polypeptide-containing neurons and nerve fibers in-sympathetic ganglia. Neuroscience 2:885–896
Hökfelt T, Elfvin L-G, Schultzberg M, Goldstein, Nilsson G (1977c) On the occurrence of substance P-containing fibers in sympathetic ganglia: Immunohistochemical evidence. Brain Res 132:29–41
Inagaki S, Kito S (1986) Peptides in the peripheral nervous system. In: Emson PC, Rossor MN, Tohyama M (eds) Progress in Brain Research, Vol 66. Elsevier Science Publishers BV, New York, pp 269–316
Kannisto P, Ekblad E, Helm G, Owman Ch, Sjöberg N-O, Stjernquist M, Sundler F, Walles B (1986) Existence and coexistence of peptides in nerves of the mammalian ovary and oviduct demonstrated by immunocytochemistry. Histochemistry 86:25–34
Klein CM, Burden HW (1987) Anatomical localization of sensory and sympathetic neurons innervating the rat ovary via the superior ovarian nerve. Anat Rec 218:p73A
Kondo H, Yui R (1981) An electron microscopic study on substance P-like immunoreactive nerve fibers in the celiac ganglion of guinea pigs. Brain Res 222:134–137
Kondo H, Yui R (1982) An electron microscopic study on VIP-like immunoreactive nerve fibers in the celiac ganglion of guinea pigs. Brain Res 237:227–231
Konishi S, Tsunoo A, Otsuka M (1979) Substance P and noncholinergic excitatory synaptic transmission in guinea pig sympathetic ganglia. Proc Jpn Acad Ser B 55:525–530
Larsson L-I, Fahrenkrug J, Schaffalitzky de Muckadell OB (1977) Vasoactive intestinal polypeptide occurs in nerves of the female genito-urinary tract. Science 197:1374–1375
Lawrence IE Jr, Burden HW (1980) The origin of the extrinsic adrenergic innervation to the rat ovary. Anat Rec 196:51–59
Liu Y-X, Kasson BG, Dahl KD, Hsueh AJW (1987) Vasoactive intestinal peptide stimulates plasminogen activator activity by cultured rat granulosa cells and cumulus-oocyte complexes. Peptides 8:29–33
Lundberg JM, Hökfelt T, Schultzberg M, Unväs-Wallensten K, Köhler C, Said SI (1979) Occurrence of vasoactive intestinal polypeptide (VIP)-like immunoreactivity in certain cholinergic neurons of the cat: Evidence from combined immunohistochemistry and acetylcholinesterase staining. Neuroscience 4:1539–1559
Lundberg JM, Hökfelt T, Änggård A, Terenius L, Eide R, Markey K, Goldstein M, Kimmel J (1982a) Organizational principles in the peripheral sympathetic nervous system: Subdivision by coexisting peptides (somatostatin-, avian pancreatic polypeptide-, and vasoactive intestinal polypeptide-like immunoreactive materials). Proc Natl Acad Sci USA 79:1303–1307
Lundberg JM, Terenius L, Hökfelt T, Martling CR, Tatemoto K, Mutt V, Polak J, Bloom S, Goldstein M (1982b) Neuropeptide Y (NPY)-like immunoreactivity in peripheral noradrenergic neurons and effects on sympathetic function. Acta Physiol Scand 116:477–480
Matthews MR (1983) The ultrastructure of junctions in sympathetic ganglia of mammals. In: Elfvin L-G (ed) Autonomic ganglia. John Wiley and Sons, New York, pp 3–26
Matthews MR, Cuello AC (1982) Substance P-immunoreactive peripheral branches of sensory neurons innervate guinea pig sympathetic neurons. Proc Natl Acad Sci USA 79:1668–1672
McNeill DL, Burden HW (1986) Neuropeptide Y and somatostatin immunoreactive perikarya in preaortic ganglia projecting to the rat ovary. J Reprod Fertil 78:727–732
McNeill DL, Burden HW (1987) Neuropeptides in sensory perikarya projecting to the rat ovary. Am J Anat 179:269–276
Ojeda WS, Chow PH (1987) Asymmetry in the ovary and uterus of the golden hamster (Mesocricetus auratus). J Reprod Fertil 80:21–23
Ojeda SR, Costa ME, Katz KH, Hersh LB (1985) Evidence for the existence of substance P in the pre-pubertal rat ovary. I. Biochemical and physiological studies. Biol Reprod 33:286–295
Ottesen B, Gram BR, Fahrenkrug J (1983) Neuropeptides in the female genital tract: Effect on vascular and non-vascular smooth muscle. Peptides 4:387–392
Papka RE, Cotton JP, Traurig HH (1985) Comparative distribution of neuropeptide tyrosine-, vasoactive intestinal polypeptide-, substance P-immunoreactive, acetylcholinesterase-positive and noradrenergic nerves in the reproductive tract of the female rat. Cell Tissue Res 242:475–490
Rao ChV, Edgerton LA (1984) Dissimilarity of corpora lutea within the same ovaries or those from right and left ovaries of pigs during the oestrous cycle. J Reprod Fertil 70:61–66
Wiebold JL Becker WC (1987) Inequality in function of the right and left ovaries and uterine horns of the mouse. J Reprod Fertil 79:125–134
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Klein, C.M., Burden, H.W. Substance P- and vasoactive intestinal polypeptide (VIP)-immunoreactive nerve fibers in relation to ovarian postganglionic perikarya in para- and prevertebral ganglia: Evidence from combined retrograde tracing and immunocytochemistry. Cell Tissue Res. 252, 403–410 (1988). https://doi.org/10.1007/BF00214383
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00214383